RecQ helicase and RecJ nuclease provide complementary functions to resect DNA for homologous recombination

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 48, 2014, Pages E5133-E5142

  Morimatsu, Katsumi ^a   Kowalczykowski, Stephen C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dna break |; Dna repair |; Helicase |; Homologous recombination |; Nuclease

Indexed keywords

COMPLEMENTARY DNA; DOUBLE STRANDED DNA; EXONUCLEASE; RECJ PROTEIN; RECQ HELICASE; SINGLE STRANDED DNA; SINGLE STRANDED DNA BINDING PROTEIN; BACTERIAL DNA; DNA BINDING PROTEIN; ESCHERICHIA COLI PROTEIN; EXODEOXYRIBONUCLEASE; RECJ PROTEIN, E COLI; RECQ PROTEIN, E COLI;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; DNA DEGRADATION; DNA DETERMINATION; DNA SUPERCOILING; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; HOMOLOGOUS RECOMBINATION; PROTEIN PROTEIN INTERACTION; BIOLOGICAL MODEL; DNA REPAIR; ESCHERICHIA COLI; GENETICS; METABOLISM; MUTATION; PLASMID;

ESCHERICHIA COLI;

DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA, BACTERIAL; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; EXODEOXYRIBONUCLEASES; HOMOLOGOUS RECOMBINATION; MODELS, GENETIC; MUTATION; PLASMIDS; RECQ HELICASES;

EID: 84915746628     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1420009111     Document Type: Article

References (70)

1. Persky NS, Lovett ST (2008) Mechanisms of recombination: Lessons from E. coli. Crit Rev Biochem Mol Biol 43(6):347-370.
2. Horii Z, Clark AJ (1973) Genetic analysis of the recF pathway to genetic recombination in Escherichia coli K12: Isolation and characterization of mutants. J Mol Biol 80(2):327-344.
3. Wang TV, Smith KC (1984) recF-dependent and recF recB-independent DNA gap-filling repair processes transfer dimer-containing parental strands to daughter strands in Escherichia coli K-12 uvrB. J Bacteriol 158(2):727-729.
4. Tseng YC, Hung JL, Wang TC (1994) Involvement of RecF pathway recombination genes in postreplication repair in UV-irradiated Escherichia coli cells. Mutat Res 315(1):1-9.
5. Kowalczykowski SC (2000) Initiation of genetic recombination and recombinationdependent replication. Trends Biochem Sci 25(4):156-165.
6. Lloyd RG, Buckman C (1985) Identification and genetic analysis of sbcC mutations in commonly used recBC sbcB strains of Escherichia coli K-12. J Bacteriol 164(2):836-844.
7. Kowalczykowski SC, Dixon DA, Eggleston AK, Lauder SD, Rehrauer WM (1994) Biochemistry of homologous recombination in Escherichia coli. Microbiol Rev 58(3): 401-465.
8. Rocha EP, Cornet E, Michel B (2005) Comparative and evolutionary analysis of the bacterial homologous recombination systems. PLoS Genet 1(2):e15.
9. Shibata T, DasGupta C, Cunningham RP, Radding CM (1979) Purified Escherichia coli recA protein catalyzes homologous pairing of superhelical DNA and single-stranded fragments. Proc Natl Acad Sci USA 76(4):1638-1642.
10. DasGupta C, Shibata T, Cunningham RP, Radding CM (1980) The topology of homologous pairing promoted by RecA protein. Cell 22(2 Pt 2):437-446.
11. Cox MM, Lehman IR (1982) recA protein-promoted DNA strand exchange. Stable complexes of recA protein and single-stranded DNA formed in the presence of ATP and single-stranded DNA binding protein. J Biol Chem 257(14):8523-8532.
12. Shinohara A, Ogawa H, Ogawa T (1992) Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69(3):457-470.
13. Sung P (1994) Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science 265(5176):1241-1243.
14. Luisi-DeLuca C, Kolodner R (1994) Purification and characterization of the Escherichia coli RecO protein. Renaturation of complementary single-stranded DNA molecules catalyzed by the RecO protein. J Mol Biol 236(1):124-138.
15. Kantake N, Madiraju MV, Sugiyama T, Kowalczykowski SC (2002) Escherichia coli RecO protein anneals ssDNA complexed with its cognate ssDNA-binding protein: A common step in genetic recombination. Proc Natl Acad Sci USA 99(24):15327-15332.
16. Umezu K, Chi NW, Kolodner RD (1993) Biochemical interaction of the Escherichia coli RecF, RecO, and RecR proteins with RecA protein and single-stranded DNA binding protein. Proc Natl Acad Sci USA 90(9):3875-3879.
17. Morimatsu K, Kowalczykowski SC (2003) RecFOR proteins load RecA protein onto gapped DNA to accelerate DNA strand exchange: A universal step of recombinational repair. Mol Cell 11(5):1337-1347.
18. Morimatsu K, Wu Y, Kowalczykowski SC (2012) RecFOR proteins target RecA protein to a DNA gap with either DNA or RNA at the 5? terminus: Implication for repair of stalled replication forks. J Biol Chem 287(42):35621-35630.
19. Shinohara A, Ogawa T (1998) Stimulation by Rad52 of yeast Rad51-mediated recombination. Nature 391(6665):404-407.
20. New JH, Sugiyama T, Zaitseva E, Kowalczykowski SC (1998) Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature 391(6665):407-410.
21. Sugiyama T, New JH, Kowalczykowski SC (1998) DNA annealing by RAD52 protein is stimulated by specific interaction with the complex of replication protein A and single-stranded DNA. Proc Natl Acad Sci USA 95(11):6049-6054.
22. Sugiyama T, Kowalczykowski SC (2002) Rad52 protein associates with replication protein A (RPA)-single-stranded DNA to accelerate Rad51-mediated displacement of RPA and presynaptic complex formation. J Biol Chem 277(35):31663-31672.
23. Volkert MR, Hartke MA (1984) Suppression of Escherichia coli recF mutations by recAlinked srfA mutations. J Bacteriol 157(2):498-506.
24. Fortin GS, Symington LS (2002) Mutations in yeast Rad51 that partially bypass the requirement for Rad55 and Rad57 in DNA repair by increasing the stability of Rad51-DNA complexes. EMBO J 21(12):3160-3170.
25. Yang H, Li Q, Fan J, Holloman WK, Pavletich NP (2005) The BRCA2 homologue Brh2 nucleates RAD51 filament formation at a dsDNA-ssDNA junction. Nature 433(7026): 653-657.
26. Jensen RB, Carreira A, Kowalczykowski SC (2010) Purified human BRCA2 stimulates RAD51-mediated recombination. Nature 467(7316):678-683.
27. Liu J, Doty T, Gibson B, Heyer WD (2010) Human BRCA2 protein promotes RAD51 filament formation on RPA-covered single-stranded DNA. Nat Struct Mol Biol 17(10): 1260-1262.
28. Handa N, Morimatsu K, Lovett ST, Kowalczykowski SC (2009) Reconstitution of initial steps of dsDNA break repair by the RecF pathway of E. coli. Genes Dev 23(10): 1234-1245.
29. Harmon FG, Brockman JP, Kowalczykowski SC (2003) RecQ helicase stimulates both DNA catenation and changes in DNA topology by topoisomerase III. J Biol Chem 278(43):42668-42678.
30. Watt PM, Louis EJ, Borts RH, Hickson ID (1995) Sgs1: A eukaryotic homolog of E. coli RecQ that interacts with topoisomerase II in vivo and is required for faithful chromosome segregation. Cell 81(2):253-260.
31. Ellis NA, et al. (1995) The Bloom's syndrome gene product is homologous to RecQ helicases. Cell 83(4):655-666.
32. Cejka P, Kowalczykowski SC (2010) The full-length Saccharomyces cerevisiae Sgs1 protein is a vigorous DNA helicase that preferentially unwinds holliday junctions. J Biol Chem 285(11):8290-8301.
33. Fiorentini P, Huang KN, Tishkoff DX, Kolodner RD, Symington LS (1997) Exonuclease I of Saccharomyces cerevisiae functions in mitotic recombination in vivo and in vitro. Mol Cell Biol 17(5):2764-2773.
34. Tsubouchi H, Ogawa H (2000) Exo1 roles for repair of DNA double-strand breaks and meiotic crossing over in Saccharomyces cerevisiae. Mol Biol Cell 11(7):2221-2233.
35. Nimonkar AV, Ozsoy AZ, Genschel J, Modrich P, Kowalczykowski SC (2008) Human exonuclease 1 and BLM helicase interact to resect DNA and initiate DNA repair. Proc Natl Acad Sci USA 105(44):16906-16911.
36. Budd ME, Choe WC, Campbell JL (1995) DNA2 encodes a DNA helicase essential for replication of eukaryotic chromosomes. J Biol Chem 270(45):26766-26769.
37. Cejka P, et al. (2010) DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature 467(7311):112-116.
38. Nimonkar AV, et al. (2011) BLM-DNA2-RPA-MRN and EXO1-BLM-RPA-MRN constitute two DNA end resection machineries for human DNA break repair. Genes Dev 25(4): 350-362.
39. Niu H, et al. (2010) Mechanism of the ATP-dependent DNA end-resection machinery from Saccharomyces cerevisiae. Nature 467(7311):108-111.
40. Lovett ST, Kolodner RD (1989) Identification and purification of a single-stranded-DNA-specific exonuclease encoded by the recJ gene of Escherichia coli. Proc Natl Acad Sci USA 86(8):2627-2631.
41. Umezu K, Nakayama K, Nakayama H (1990) Escherichia coli RecQ protein is a DNA helicase. Proc Natl Acad Sci USA 87(14):5363-5367.
42. Harmon FG, Kowalczykowski SC (2001) Biochemical characterization of the DNA helicase activity of the Escherichia coli RecQ helicase. J Biol Chem 276(1):232-243.
43. Honigberg SM, Gonda DK, Flory J, Radding CM (1985) The pairing activity of stable nucleoprotein filaments made from recA protein, single-stranded DNA, and adenosine 5?-(ã-thio)triphosphate. J Biol Chem 260(21):11845-11851.
44. Roman LJ, Kowalczykowski SC (1986) Relationship of the physical and enzymatic properties of Escherichia coli recA protein to its strand exchange activity. Biochemistry 25(23):7375-7385.
45. Han ES, et al. (2006) RecJ exonuclease: Substrates, products and interaction with SSB. Nucleic Acids Res 34(4):1084-1091.
46. Shereda RD, Reiter NJ, Butcher SE, Keck JL (2009) Identification of the SSB binding site on E. coli RecQ reveals a conserved surface for binding SSB's C terminus. J Mol Biol 386(3):612-625.
47. Shereda RD, Bernstein DA, Keck JL (2007) A central role for SSB in Escherichia coli RecQ DNA helicase function. J Biol Chem 282(26):19247-19258.
48. Hsieh P, Camerini-Otero CS, Camerini-Otero RD (1992) The synapsis event in the homologous pairing of DNAs: RecA recognizes and pairs less than one helical repeat of DNA. Proc Natl Acad Sci USA 89(14):6492-6496.
49. Shen P, Huang HV (1986) Homologous recombination in Escherichia coli: dependence on substrate length and homology. Genetics 112(3):441-457.
50. Luisi-DeLuca C, Lovett ST, Kolodner RD (1989) Genetic and physical analysis of plasmid recombination in recB recC sbcB and recB recC sbcA Escherichia coli K-12 mutants. Genetics 122(2):269-278.
51. Sawitzke JA, Stahl FW (1992) Phage lambda has an analog of Escherichia coli recO, recR and recF genes. Genetics 130(1):7-16.
52. Stahl FW, Kobayashi I, Stahl MM (1985) In phage lambda, cos is a recombinator in the red pathway. J Mol Biol 181(2):199-209.
53. Sawitzke JA, Stahl FW (1997) Roles for lambda Orf and Escherichia coli RecO, RecR and RecF in lambda recombination. Genetics 147(2):357-369.
54. Sawitzke JA, Stahl FW (1994) The phage lambda orf gene encodes a trans-acting factor that suppresses Escherichia coli recO, recR, and recF mutations for recombination of lambda but not of E. coli . J Bacteriol 176(21):6730-6737.
55. Alatossava T, Jütte H, Kuhn A, Kellenberger E (1985) Manipulation of intracellular magnesium content in polymyxin B nonapeptide-sensitized Escherichia coli by ionophore A23187. J Bacteriol 162(1):413-419.
56. Lavery PE, Kowalczykowski SC (1992) Enhancement of recA protein-promoted DNA strand exchange activity by volume-occupying agents. J Biol Chem 267(13): 9307-9314.
57. Wakamatsu T, et al. (2010) Structure of RecJ exonuclease defines its specificity for single-stranded DNA. J Biol Chem 285(13):9762-9769.
58. Williams KR, Spicer EK, LoPresti MB, Guggenheimer RA, Chase JW (1983) Limited proteolysis studies on the Escherichia coli single-stranded DNA binding protein. Evidence for a functionally homologous domain in both the Escherichia coli and T4 DNA binding proteins. J Biol Chem 258(5):3346-3355.
59. Cannavo E, Cejka P, Kowalczykowski SC (2013) Relationship of DNA degradation by Saccharomyces cerevisiae exonuclease 1 and its stimulation by RPA and Mre11-Rad50-Xrs2 to DNA end resection. Proc Natl Acad Sci USA 110(18):E1661-E1668.
60. Nimonkar AV, Sica RA, Kowalczykowski SC (2009) Rad52 promotes second-end DNA capture in double-stranded break repair to form complement-stabilized joint molecules. Proc Natl Acad Sci USA 106(9):3077-3082.
61. Zhu Z, Chung WH, Shim EY, Lee SE, Ira G (2008) Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134(6):981-994.
62. Gravel S, Chapman JR, Magill C, Jackson SP (2008) DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev 22(20):2767-2772.
63. Karow JK, Chakraverty RK, Hickson ID (1997) The Bloom's syndrome gene product is a 3?-5? DNA helicase. J Biol Chem 272(49):30611-30614.
64. Nicolette ML, et al. (2010) Mre11-Rad50-Xrs2 and Sae2 promote 5? strand resection of DNA double-strand breaks. Nat Struct Mol Biol 17(12):1478-1485.
65. Szankasi P, Smith GR (1992) A DNA exonuclease induced during meiosis of Schizosaccharomyces pombe. J Biol Chem 267(5):3014-3023.
66. Imamura O, Campbell JL (2003) The human Bloom syndrome gene suppresses the DNA replication and repair defects of yeast dna2 mutants. Proc Natl Acad Sci USA 100(14):8193-8198.
67. Mimitou EP, Symington LS (2008) Sae2, Exo1 and Sgs1 collaborate in DNA doublestrand break processing. Nature 455(7214):770-774.
68. Harmon FG, Kowalczykowski SC (1998) RecQ helicase, in concert with RecA and SSB proteins, initiates and disrupts DNA recombination. Genes Dev 12(8):1134-1144.
69. Lohman TM, Green JM, Beyer RS (1986) Large-scale overproduction and rapid purification of the Escherichia coli ssb gene product. Expression of the ssb gene under lambda PL control. Biochemistry 25(1):21-25.
70. Morimatsu K, Horii T, Takahashi M (1995) Interaction of Tyr103 and Tyr264 of the RecA protein with DNA and nucleotide cofactors. Fluorescence study of engineered proteins. Eur J Biochem 228(3):779-785.